Surgery Outcomes of Lamellar Macular Eyes with or without Lamellar Hole-Associated Epiretinal Proliferation: A Meta-Analysis

doi:10.21203/rs.2.18331/v4

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Surgery Outcomes of Lamellar Macular Eyes with or without Lamellar Hole-Associated Epiretinal Proliferation: A Meta-Analysis

https://doi.org/10.21203/rs.2.18331/v4

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published 25 Aug, 2020

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Background: To compare the visual outcomes and rate of restored ellipsoid zone (REZ) after surgery of lamellar macular hole (LMH) with and without lamellar hole-associated epiretinal proliferation (LHEP).

Method: Publications up to November 2019 that compared the outcomes of LMH patients with and without LHEP who were managed by surgery were included. Forest plots were created using a weighted summary of proportion meta-analysis. A random effects mode was used and I2 heterogeneity estimates were calculated. Sensitivity analysis was carried out to evaluate the stability of the meta-analysis.

Result: Eight pertinent publications studying a total of 176 eyes without LHEP and 173 eyes with LHEP were identified. They were all retrospective studies and had a mean follow-up of at least 6 months. In all studies, the best corrected visual acuity (BCVA) had no significant differences before surgery and improved in both groups, and in two studies the post-operative BCVA had no significant differences between two groups. The rate of REZ were different among studies included. Meta-analytic pooling of the improved BCVA between with and without LHEP groups was 0.18 (95 % CI, 0.10 to 0.26; P< 0.01), and the pooled data revealed an odd ratio of 0.80 (95% CI, 0.26 to 2.44; p = 0.69) in the rate of REZ, comparing the group without LHEP and the group with LHEP. In conclusion, patients without LHEP had better postoperative BCVA than patients with LHEP. No significant difference was found in REZ among the two groups.

Ophthalmology

lamellar macular hole

lamellar hole-associated epiretinal proliferation

surgery

best corrected visual acuity

ellipsoid zone

Lamellar macular hole (LMH) is a partial-thickness loss of foveal tissue, firstly described by Gass based on biomicroscopic and angiographic findings in a case[1]. The formation of LMH can be due to cystoid macular edema, contraction of the perifoveal epiretinal membrane and virteous traction[2]. The diagnosis of LMH was redefined in 2006 by Witkin et al. with characteristics as follows: (1) irregular foveal contour; (2) break in the inner fovea; (3) intraretinal split; and (4) intact foveal photoreceptors[2].

With the development of ultrahigh-resolution optical coherence tomography (UHR-OCT), the structure of LMH has been observed more clearly. Epiretinal membranes (ERM) are visualized on UHR-OCT in most cases of LMH and represented as trapped vitreous or posterior hyaloid. There are two types of ERM, tractional ERM (T ERM) and lamellar hole-associated epiretinal proliferation (LHEP) which is also named as thick ERM and dense ERM. Based on OCT, T ERM is observed as a dense reflective line above retina, while LHEP is homogenous medium with much lower reflectivity. Meanwhile, T ERM has stronger contractile properties compared with LHEP [3]. These two kinds of ERM can occur in LMH patients simultaneously or separately, and T ERM occurs more often than LHEP.

In terms of treating LMH, surgery is still a controversial choice. Pars plana vitrectomy with internal limiting membrane (ILM) peeling is the most common method and has been reported to be useful in most patients with LMH, especially those with significantly low visual acuity [4-6]. However, this operation still has some risks, as some patients have an unsatisfactory outcome and develop into full thickness macular hole (FTMH) after surgery. Moreover, the natural progress of LMH is stable and observation can still be helpful for some patients [7].

To figure out the differences in prognosis among patients with or without LHEP, some previous studies focused on the surgical outcomes of patients with and without LHEP, but their results were inconsistent. Based on these studies, we aimed to compare patients with and without LHEP with the outcomes of the surgery.

We searched the PubMed, Medline, Embase and Clinical-trails for studies in comparing surgical outcomes of LMH patients with and without LHEP. All studies included were retrospective studies. We identified relevant studies using the terms “Lamellar macular hole”, or “LMH”, or “epiretinal membrane”, or “ERM”, or “lamellar hole-associated epiretinal proliferation”, or “LHEP”, and “surgery” or “operation” or “vitrectomy”.

Study selection

For all studies included, the inclusion criteria were if study: 1) compared LMH patients with and without LHEP; 2) provided specific numbers for patients in each group; 3) reported the best corrected visual acuity (BCVA) both before and after operation; 4) took a standard pars plana vitrectomy combining with ERM and ILM peeling; 5) had a mean follow-up of at least 6 months. Exclusion criteria included having: 1) inadequate record of surgery progress and postoperative BCVA at ≥ 6 months; 2) patients developed into FTMH before surgery.

Validity assessment

Our search identified 272 studies, of which 8 articles fulfilled our inclusion criteria. Figure 1 summarized the process of the study selection. NOS (Newcastle-Ottawa Scale) was used by two investigators separately to score the quality of all included studies, and the total score of every study was equal or greater than 7.

Data abstraction

All the information in the involved studies were extracted by two investigators separately, including basic characteristics, surgery method, preoperative and postoperative data using a standardized protocol. Disagreements were resolved by consensus.

Quantitative data synthesis

The summary odds ratios (OR) of LMH patients with and without LHEP with 95% confidence intervals (95%CI) were also calculated, and the weighted mean difference （WMD） was calculated with the 95 % CI for BCVA. A P value < 0.05 was considered to be statistically significant.

Both fixed effect and random effects models were used to pool studies. When I² index, which measures the extent of the heterogeneity, was less than 50%, the final conclusions were drawn from the results of the fixed effects model, otherwise using random effects model. Funnel plots was used to identify the potential publication bias. Sensitivity analysis was carried out to evaluate the stability of the meta-analysis by omitting one study each time.

All statistical analyses were conducted with Review Manager (version 5.2; Cochrane Collaboration, Oxford, UK; http://ims.cochrane.org/revman) and STATA software (version 11.0; Stata Corp LP, College Station, TX).

Characteristics of the available studies

A total of 287 records were retrieved from the electronic database search (Figure 1). After removing duplications and articles written in other languages, 155 articles were left. By reading the titles and abstracts, 14 researches related to LHEP and surgery outcomes were reserved. Two studies included patients with FTMH were excluded [8, 9], and a study recruited LMH patients with high myopia was also excluded [10]. Meanwhile, two study with incomplete information were excluded [11, 12]. In addition, another study was excluded for it was an observational study without surgery [3]. Finally, 8 studies with 176 eyes without LHEP and 173 eyes with LHEP were included [13-20].

Outcomes of meta-analysis

No significant heterogeneity was observed in the comparing model of BCVA (I²=22%, P=0.28) and restored ellipsoid zone (REZ) (I²=48%, P=0.16). So fixed-model analysis was used in the meta-analysis. The WMD in the improved logarithm of the minimum angle of resolution BCVA between with and without LHEP groups was 0.18 (95 % CI, 0.10 to 0.26; P< 0.01). Meta-analysis showed statistically significant difference (P= 0.02). Only three studies reported the status of ellipsoid zone before and after surgery. The pooled data revealed an OR of 0.80 in the rate of restored ellipsoid zone, comparing the group with LHEP and the group without LHEP. It was not statistically significant at the 95% level (95% CI, 0.26 to 2.44; p = 0.69) (figure 2).

To assess potential publication bias in the meta-analysis, funnel plots were visually inspected, and no funnel plot asymmetry was visualized (Figure 3). By egger test, no publication bias existed in the studies with BCVA reported (P=0.889). Sensitivity analysis was conducted to evaluate the influence of individual data on the pooled results of BCVA. The statistical findings of BCVA did not change by removing any one of the studies (Figure 4).

The present study found the surgery outcomes of LMH patients with and without LHEP had significant difference. Patients with LHEP were more likely to gain restored ellipsoid zone after surgery but had lower postoperative BCVA.

The existence of ERM has been detected for several decades, while the pathogenesis and category of it are still unclear. T ERM is tractional and the retinal surface under it is usually plicate. The LMH associated with T ERM always has short diameter and shallow cleft, limited in the inner part of retina and described as “high hat” by Andrea et al. In contrast, LHEP is an atypical ERM with no traction and the LMH associated with it is larger and deeper [21]. In a previous study, glial cells and hyalocytes were found in both these two kinds of membranes, while α-SAM was only found in T ERM, explaining the tractional ability of T ERM [22].

The origin of LHEP is not clear but there are two main theories. Firstly, as LHEP has abundant clusters of fibrous long-spacing collagen, fibroblasts and hyalocytes, it is believed that the posterior detachment of vitreous body, which induce anterior and tangential traction, plays a role in the formation of ERM [16, 22]. Secondly, the finding of the cystic spaces in LHEP, which is due to the leakage of fluid from retinal vessels within it, suggesting LEHP possesses characteristics similar to that of the middle retinal layers and probably originates from there [3]. The proof that yellow color of LHEP is xanthophyll mainly produced by muller cells further certifies the relationship between LHEP and the middle retinal layers [23].

According to the results of present study, less BCVA could be regained in patients with LHEP after surgery compared with those without LHEP. This result is in consistence with most of the previous studies, which also found LMH or FTMH eyes with LHEP had worse visual outcome after surgery [8, 13, 14, 24]. This may be because the destroy of retina was severer in eyes with LHEP than without LHEP. However, there were also some studies reported similar surgery outcomes of eye with LHEP [10, 12, 15, 16]. As there are no significant differences of preoperative BCVA (<20/40), surgery method (ILM and ERM peeling) and time of follow-up (>6 months) among the two kinds of studies, more study with longer follow up is required for detecting whether poorer visual outcome is associated with LHEP.

Though many studies have reported the positive association between the REZ and postoperative BVCA [25, 26], there was no significant differences of REZ existing between with and without LHEP groups. There were studies reported that though the defection of ellipsoid zone before surgery was associated with worse postoperative BCVA, its restoration showed no direct association with functional recover [5, 27]. Meanwhile, several influence factors also need to be taken into consideration, including the different preoperative BCVA and limited number of studies could be involved. In the study, which showed more eyes with LHEP get restored after surgery, patients all had preoperative BCVA lower than 20/40 [13], while in other two studies patients with wider range of BCVA were included [14, 15].

Six of all included studies had patients with standard pars plana vitrectomy with traditional ERM and ILM peeling [13-17, 19]. A new surgery method has been used in other two studies for LHM patients with ERM [18, 20]. Comparing with the regular surgery method, the main difference is about the disposition of ERM and ILM. Instead of peeling the membrane, in the new method, ERM was double inverted and ILM was flapped [28, 29]. This kind of surgery can retain LHEP and promote the recovery of LHM, and a study indicated that the development of LHEP might be a recovery progress of LMH [15]. This newly surgical method and its positive outcomes further raise a doubt in the necessity of taking surgery for LHM patients with ERM.

There are some limitations in this study that need to be mentioned. Firstly, the number of studies involved is small and more studies are required for extended exploration. Secondly, the number of patients with cataract were only stated in two studies, and the different number of patients with combined phacoemulsification and intraocular lens implantation can influence the outcome of BCVA. Thirdly, there were slight differences in the choice of the gas for the final tamponade, either air, sulphur hexafluoride or perfluoropropane gas.

In conclusion, this study pooled the postoperative outcomes of LMH patients with and without LHEP and found that the postoperative BCVA of patients without LHEP was better than patients with LHEP, and there was no significant difference of REZ among the two groups.

BCVA, best corrected visual acuity; CI, confidence intervals; ERM, epiretinal membranes; DLMH, Diameter of Lamellar Macular Hole; FTMH, full thickness macular hole; ILM, internal limiting membrane; LHEP, lamellar hole-associated epiretinal proliferation; LMH, lamellar macular hole; NOS, Newcastle - Ottawa Scale; OR, odds ratios; REZ, restored ellipsoid zone; SFT, Shortest Foveal Thickness; T ERM, tractional epiretinal membranes; UHR-OCT, ultrahigh-resolution optical coherence tomography; WMD, weighted mean difference

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests

Funding

Not applicable

Authors' contributions

MZ and LQ contributed to the study design. HY X and YF Z contributed to the data collection and analysis. HY X contributed to the writing of this manuscript. All authors read and approved this manuscript.

Acknowledgements

Not applicable

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Table 1. Demographic characteristics of the included studies

Author	Barbara et al.			Lai et al.	Ko et al.			Choi et al.		Ho et al.		Kosuke et al.	Marta et al.			Francesco et al.
Year	2011			2015	2016			2017		2019		2019	2019			2020
Country	Germany			China	Korea			USA		China		Japan				Italy
Study design	retrospective			retrospective	retrospective			retrospective		retrospective		retrospective	retrospective			prospective
Study period	2008-2010			2009-2013	2011-2014			2009-2015		2013-2016		2010-2016	2010-2017			2015-2017
Surgery	Vitrectomy ILM/ERM peeling			Vitrectomy ILM/ERM peeling	Vitrectomy ILM/ERM peeling			Vitrectomy ILM/ERM peeling		Vitrectomy ILM/ERM peeling or LHEP embedding		Vitrectomy ILM peeling LHEP embedding	Vitrectomy ILM/ERM peeling			Vitrectomy ILM/ERM peeling
Follow-up	6 months			> 12 months	> 6 months			> 6 months		> 19 months		> 12 months	> 6 months			6 months
Without LHEP
Number		6	24			58	11		-			-		77				-
Age (Y)		67.7 ± 12.9	59.8 ± 8.9			64.4 ± 9.5	68.6 ± 8.8		-			-		67 ± 8.9				-
Gender (M/F)		1/5	9/15			9/16	-							-
FT (μm)		-	146.9 ± 51.2			154.0 ± 24.7	166.7 ± 62.0		-			-		279.1 ± 108				-
DLMHI (μm)		-	-			450.4 ± 201.8	308.2 ± 121.2		-			-		-				-
AL (mm)		-	-			23.66 ± 1.59	-		-			-		-				-
With LHEP
Number		13	19			15	11			31	34				26		24
Age (Y)		73.9 ± 12.9	60.2 ± 11.2			67.4 ± 9.5	69.9 ± 13.6			67.7 ± 8.7	69.6 ± 10.1				67 ± 8.9		72.1 ± 8.3
Gender (M/F)		8/5	9/10			4/11	-			6/25	12/22				-		15/9
FT (μm)		-	98.4 ± 35.0			116.7 ± 38.1	96.3 ± 33.2			-	-				224 ± 66		-
DLMHI (μm)		-	-			613.5 ± 197.3	334.1 ± 139.8			-	-				-		-
AL (mm)		-	-			24.12 ± 1.84	-			-	24 (< 26), 10 (26≦)				-		-

Abbreviations: AL, Axial Length; DLMHI, Diameter of Lamellar Macular Hole at the ILM level (pre-operation); ERM, Epiretinal Membrane; FT, Foveal Thickness (pre-operation); ILM, Internal Limited Membrane; LHEP, Lamellar Hole-Associated Epiretinal Proliferation; M/F, male/female.

Table 2. Ophthalmic information of involved studies

Author		Barbara et al.	Lai et al.	Ko et al.		Choi et al.		Ho et al.	Kosuke et al.		Marta et al.	Francesco et al.
BCVA (pre-operation)	Without LHEP	0.40 ± 0.20	0.72 ± 0.32	0.30 ± 0.26	0.48 ± 0.18		-			-	0.38 ± 0.19	-
	With LHEP	0.40 ± 0.20	0.79 ± 0.37	0.38 ± 0.38	0.50 ± 0.25		0.37 ± 0.27			0.31 ± 0.25	0.56 ± 0.19	0.44 ± 0.16
BCVA (post-operation)	Without LHEP	0.20 ± 0.30	0.43 ± 0.44	0.10 ± 0.10	0.16 ± 0.16		-			-	0.18 ± 0.17	-
	With LHEP	0.20 ± 0.20	0.45 ± 0.39	0.33 ± 0.40	0.40 ± 0.29		0.17 ± 0.21			0.10 ± 0.25	0.39 ± 0.28	0.17 ± 0.13
EZD (pre-operation)	Without LHEP	-	9 (24)	0 (42)	3 (11)		-			-	11 (77)	-
	With LHEP	-	13 (19)	2 (10)	10 (11)		10 (33)			15 (34)	13 (26)	-
EZD (post-operation)	Without LHEP	-	8 (24)	2 (42)	2 (11)		-			-	6 (77)	-
	With LHEP	-	7 (19)	2 (10)	8 (11)		4 (33)			8 (34)	12 (26)	-
CRT (pre-operation) (μm)	Without LHEP	-	-	-	166.7 ± 62.0		-			-	-	-
	With LHEP	-	-	-	96.3 ± 33.2		-			123.2 ± 42.6	-	146 ± 34
CRT (post-operation) (μm)	Without LHEP	-	-	-	230.6 ± 103.3		-			-	-	-
	With LHEP	-	-	-	205.6 ± 112.9		-			191.2 ± 45.3	-	272 ± 24

Abbreviations: BCVA, Best corrected visual acuity; CRT, Central Retinal Thickness; EZD, Ellipsoid zone destruction; LHEP, Lamellar hole-associated epiretinal proliferation.

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Editorial decision: Major revision
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Surgery Outcomes of Lamellar Macular Eyes with or without Lamellar Hole-Associated Epiretinal Proliferation: A Meta-Analysis

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